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1.A.1 The Voltage-gated Ion Channel (VIC) Superfamily

Proteins of the VIC family are ion-selective channel proteins found in a wide range of bacteria, archaea, eukaryotes and viruses. They are often homo- or heterooligomeric structures with several dissimilar subunits (e.g., α1-α2-δ-β Ca2+ channels, αβ1β2 Na+ channels or (α)4-β K+ channels), but the channel and the primary receptor is usually associated with the α (or α1) subunit. Functionally characterized members are specific for K+, Na+ or Ca2+. The K+ channels usually consist of homotetrameric structures with each α-subunit possessing six transmembrane spanners (TMSs). Many voltage-sensitive K+ channels function with β-subunits that modify K+ channel gating. These nonintegral β-subunits are oxidoreductases that coassemble with the tetrameric α-subunits in the endoplasmic reticulum and remain tightly adherent to the α-subunit tetramer. The high resolution β-subunit structure is available (Gulbis et al., 1999). Non-homologous β-subunits of Na+ and Ca2+ channels function in regulation (Hanlon and Wallace, 2002).

The α subunits of the Ca2+ and Na+ channels are about four times as large as the K+ channel α-subunits and possess 4 units, each with 6 TMSs separated by a hydrophilic loop, for a total of 24 TMSs. These large channel proteins form heterotetrameric-unit structures equivalent to the homotetrameric structures of most K+ channels. All four units of the Ca2+ and Na+ channels are homologous to the single unit in the homotetrameric K+ channels. Ion flux via the eukaryotic channels is generally controlled by the transmembrane electrical potential (hence the designation, voltage-sensitive) although some are controlled by ligand or receptor binding. The 6 TMS VIC family members have a gating charge transfer center in the voltage sensors (Tao et al., 2010).  Structural aspects of the calcium channels, revealing the architectural features that underlie their feedback regulatory mechanisms have been reviewed (Minor and Findeisen 2010). 

There are four known K+ channel families in mammals (humans): (1) The voltage dependent K+ channels designated as Kv channels, which consist of twelve subfamilies. (2) The two pore domain channels, the K2P, which consist of fourteen subfamilies. (3) The calcium activated K+ channels, KCa channels, which consist of five subfamilies. (4) The inward rectifier K+ channel, the Kir, which include seven subfamilies, designated Kir 1 - Kir 7 with fifteen members. G-protein coupled receptors (GPCRs) modulate a number of K+ channels. The most intensively studied and characterized are the K+ inward rectifier Kir 3 subfamily (Kir3.1-Kir3.4) (Gohar, 2006). 

BK-type Ca2+ channels and lipid phosphatases have a transmembrane voltage sensor domain (VSD) that moves in response to physiological variations of the membrane potential to control their activities. However, VSD movements and coupling to the channel or phosphatase activities may differ depending on various interactions between the VSD and its host molecules (Cui 2010). BK-type voltage, Ca²+ and Mg²+ activated K+ channels contain the VSD and a large cytosolic domain (CTD) that binds Ca²+and Mg²+. VSD movements are coupled to BK channel opening with a unique allosteric mechanism and are modulated by Ca²+ and Mg²+ binding via interactions between the channel pore, VSD and CTD. It is energetically advantageous for the pore to be controlled by multiple stimuli (Cui 2010).

The erg or Kv11 (according to the new nomenclature) is a subfamily of the voltage-dependent K+ channel superfamily and includes three members: Kv11.1 (erg1), Kv11.2 (erg2) and Kv11.3 (erg3) channels. The most studied member of this subfamily is Kv11.1 that regulates the duration of the cardiac action potential. Mutations in this channel have been associated with cardiac arrhythmias and sudden death (Bronstein-Sitton, 2006).

Five types of Ca2+ channels are expressed in the CNS of mammals: The L-type (Cav1), N-type (Cav2.2), P/Q-type (Cav2.1), R-type (Cav2.3), and the T-type (Cav3). Each Cav channel is a multimeric protein composed of a pore forming α1 subunit and the auxiliary β (Cavβ), α2δ and γ subunits. There are four known Cavβ subunits, in addition to four α2δ subunits and eight γ subunits. The best characterized Ca2+ channels that are regulated by GPCRs are the N-type and the P/Q-type which have significant roles in neuronal communication. This mechanism is the basis of synaptic modulation caused by endogenous hormones as well as exogenously applied agents (such as analgesia caused by morphine). The identification of the types of Ca2+ channels that are modulated by GPCRs was enabled by the use of specific toxins: ω-Conotoxin GVIA for the N-type channels and ω-Agatoxin-IVA for the P/Q-type channels. Many Ca2+ channels are regulated by GPCRs (Gohar, 2006). Endodgenous membrane phosphatidylinositol 4,5-biphosphate, PIP2, activates high voltage activated L-, N- and P/Q type Ca2+ channels, and PIP2 depletion inhibits these Ca2+ channels (Suh et al., 2010).

In type-2 diabetes, the tight link between glucose sensing and insulin secretion is impaired due to mutations in a KATP channel. K+ channels that are sensitive to ATP are plasma membrane protein complexes composed of four Kir6.2 (KCNJ11) pore-forming subunits surrounded by four SUR1 (sulphanylurea receptor, of the ABC superfamily) auxiliary subunits. These protein complexes sense the amount of glucose entering a beta cell in the pancreas since the activity of KATP channels depends on the amount of ATP in the cytoplasm, which in turn depends on the amount of glucose absorbed by the beta cell. The activity of KATP channels is negatively correlated to the amount of ATP. KATP channels are the main channels that are open during resting conditions. Closure of KATP channels by increased ATP concentrations leads to membrane depolarization, which causes opening of voltage dependent Ca2+ (Cav) channels, leading to Ca2+ influx. The main Cav channels that control insulin secretion are L-type channels of the Cav1 subfamily (Cav1.2 and/or Cav1.3) (Cherki et al., 2006).

Ion channelopathies are inherited diseases in which alterations in control of ion conductance through the central pore of ion channels impair cell function, leading to periodic paralysis, cardiac arrhythmia, renal failure, epilepsy, migraine and ataxia (Kullmann and Waxman, 2010). However, Sokolov et al. (2007) have shown that, in contrast with this well-established paradigm, three mutations in gating-charge-carrying arginine residues in an S4 segment of NaV1.4 (TC #1.A.1.10.4) that cause hypokalaemic periodic paralysis induce a hyperpolarization-activated cationic leak through the voltage sensor of the skeletal muscle NaV1.4 channel. This 'gating pore current' is active at the resting membrane potential and closed by depolarizations that activate the voltage sensor. It has similar permeability to Na+, K+ and Cs+, but the organic monovalent cations tetraethylammonium and N-methyl-D-glucamine are much less permeant. The inorganic divalent cations Ba2+, Ca2+ and Zn2+ are not detectably permeant and block the gating pore at millimolar concentrations. The results reveal gating pore current in naturally occurring disease mutations of an ion channel and show a clear correlation between mutations that cause gating pore current and hypokalemic periodic paralysis.

Several putative K+-selective channel proteins of the VIC family have been identified in prokaryotes. The structures of two of them, the 2 TMS voltage-insensitive KcsA K+ channel of Streptomyces lividans and the 6 TMS KvAP voltage-sensitive K+ channel of Aeropyrum pernix, have been solved to 3.2 Å resolution (TC #1.A.1.1.1 and 1.A.1.17.1, respectively) (Cuello et al., 2004; Doyle et al., 1998; Jiang et al., 2003a,b; Ruta et al., 2003). Both proteins possess four identical subunits, each with two transmembrane helices, arranged in the shape of an inverted teepee or cone, forming the channel. The cone cradles the 'selectivity filter' P domain in its outer end. The narrow selectivity filter is only 12 Å long, whereas the remainder of the channel is wider and lined with hydrophobic residues. The first TMS (S1) is at the contact interface between the voltage sensing and pore domains (Cuello et al., 2004). A large water-filled cavity and helix dipoles stabilize K+ in the pore. The selectivity filter has two bound K+ ions about 7.5 Å apart from each other. Ion conduction is proposed to result from a balance of electrostatic attractive and repulsive forces. Evolutionary relationships between K+ channels and certain K+:cation symporters has been reviewed and discussed (Durell et al., 1999).

KcsA channels twist around the axis of the pore. Conformational changes are prevented by an open-channel blocker, tetrabuthylammonium. Random clockwise and counterclockwise twisting in the range of several tens of degrees originate in the transmembrane domain and are transmitted to the cytoplasmic domain. This twisting motion may play a role in gating (Shimizu et al., 2008). This coupling suggests a mechanical interplay between the transmembrane and cytoplasmic domains.

The open-state conformation of the KcsA K+ channel has been studied using the Monte Carlo normal mode following simulations. Gating involves rotation and unwinding of the TM2 bundle, lateral movement of the TM2 helices away from the channel axis, and disappearance of the TM2 bundle. The open-state conformation of KcsA exhibits a wide inner vestibule, with a radius approximately 5-7 Å and inner helices bent at the A98-G99 hinge. Computed conformational changes demonstrate that spin labeling and X-ray experiments illuminate different stages in gating: transition begins with clockwise rotation of the TM2 helices ending at a final state with the TM2 bend hinged near residues A98-G99. The concordance between the computational and experimental results provides atomic-level insight into the structural rearrangements of the channel's inner pore (Miloshevsky and Jordan, 2007).

Interconversion between conductive and non-conductive forms of the K+ channel selectivity filter underlies a variety of gating events. Cuello et al. (2010) reported the crystal structure of the Streptomyces lividans K+ channel, KcsA, in its open-inactivated conformation. They investigated the mechanism of C-type inactivation gating at the selectivity filter from channels 'trapped' in a series of partially open conformations. Five conformer classes were identified with openings ranging from 12 Å in closed KcsA to 32 Å when fully open. A correlation was observed between the degree of gate opening and the conformation and ion occupancy of the selectivity filter. A gradual filter backbone reorientation leads first to a loss of the S2 ion binding site and a subsequent loss of the S3 binding site, presumably abrogating ion conduction. 

The archaeal voltage-dependent K+ channel (TC #1.A.1.17.1) has been characterized (Ruta et al., 2003). It exhibits the properties of a classical neuronal K+ channel including structural conservation in the voltage sensor as revealed by specific high affinity tarantula venom toxin binding. This toxin evolved to inhibit animal Kv channels.

Three other bacterial VIC family channels have been characterized functionally. One is the 2 TMS LctB channel of Bacillus stearothermophilus (TC #1.A.1.1.2; Wolters et al., 1999), the second is the 6 TMS Kch channel of E. coli (TC #1.A.1.13.1; Ungar et al., 2001), and the third is the Bacillus halodurans 6 TMS voltage-gated Na+ channel (TC #1.A.1.14.1; Ren et al., 2001). This last-mentioned protein, called NaChBac, is most similar in sequence to voltage-gated Ca2+ channels (TC #1.A.1.11.1-3). A family of these 6 TMS voltage-gated Na+ channels (22-54% identical) is widespread in bacteria, suggesting a fundamental function (Koishi et al., 2004). These three proteins are all distantly related to KcsA of S. lividans, particularly LctB. Kch has been shown to form tetramers that may function to maintain the membrane potential in the early stationary phase of growth (Ungar et al., 2001).

Prokaryotic voltage-gated sodium channels form homotetramers with each subunit contributing six transmembrane α-helices (S1-S6). Helices S5 and S6 form the ion-conducting pore, and helices S1-S4 function as the voltage sensor with helix S4 thought to be the essential element for voltage-dependent activation. The crystal structures have provided insight into voltage-gated K channels, revealing a characteristic domain arrangement in which the voltage sensor domain of one subunit is close to the pore domain of an adjacent subunit in the tetramer. Shimomura et al. (2011) showed that the domain arrangement in NaChBac, (TC# 1.A.1.14.1), is similar to that in voltage-gated K+ channels. The domain arrangement and vertical mobility of helix S4 in NaChBac indicated that the structure and mechanism of voltage-dependent activation in prokaryotic Na+ channels are similar to those in canonical voltage-gated K+ channels (Shimomura et al., 2011).

In eukaryotes, each VIC family channel type has several subtypes based on pharmacological and electrophysiological data. Thus, there are six types of Ca2+ channels (L, N, P, Q, R and T). There are at least ten types of K+ channels, each responding in different ways to different stimuli: voltage-sensitive [Ka, Kv, Kvr, Kvs and Ksr], Ca2+-sensitive [BKCa, IKCa and SKCa] and receptor-coupled [KM and KACh+ channels (I, II, III, μ1, H1 and PN3). Cyclic nucleotide-responsive channels (families 1.A.1.4 and 1.A.1.5) contain centrally located CAP_ED domains, although the cyclic nucleotide regulatory properties have only been reported for family 1.A.5, not 1.A.4. Tetrameric channels from both prokaryotic and eukaryotic organisms are known in which each α-subunit possesses 2 TMSs rather than 6, and these two TMSs are homologous to TMSs 5 and 6 of the 6 TMS unit found in the voltage-sensitive channel proteins. KcsA of S. lividans is an example of such a 2 TMS channel protein. These channels may include the KNa (Na+-activated) and KVol (cell volume-sensitive) K+ channels, as well as distantly related channels such as the Tok1 K+ channel of yeast. The TWIK-1 and -2, TREK-1, TRAAK, and TASK-1 and -2 K+ channels all exhibit a duplicated 2 TMS unit and may therefore form a homodimeric channel. About 50 of these 4 TMS proteins are encoded in the C. elegans genome. Because of insufficient sequence similarity with proteins of the VIC family, inward rectifier K+ IRK channels (ATP-regulated; G-protein-activated) which possess a P domain and two flanking TMSs are placed in a distinct family (TC #1.A.2). However, substantial sequence similarity in the P region suggests that they are homologous. The β, γ, and δ subunits of VIC family members, when present, frequently play regulatory roles in channel activation/deactivation.

The function of voltage-dependent K+ channels is dependent on the negatively charged phosphodiester of phospholipid molecules. A non-voltage-dependent K+ channel does not exhibit the same dependence. It was proposed that the phospholipid membrane, by providing stabilizing interactions between positively charged voltage-sensor arginine residues and negatively charged lipid phosphodiester groups, provides an appropriate environment for the energetic stability and operation of the voltage-sensing machinery. The usage of arginine residues in voltage sensors is an adaptation to the phospholipid composition of cell membranes (Schmidt et al., 2006). The X-ray structure of a voltage-dependent K+ channel (Kv) can explain charge stabilization within the membrane and thus suggests the mechanism for coupling voltage-sensor movements to pore gating (Long et al., 2007).

Voltage-gated ion channels derive their voltage sensitivity from the movement of specific charged residues in response to a change in transmembrane potential. Several studies on mechanisms of voltage sensing in ion channels support the idea that these gating charges move through a well-defined permeation pathway. This gating pathway in a voltage-gated ion channel can also be mutated to transport free cations, including protons (Chanda and Chanda and Bezanilla, 2008). The discovery of proton channels homologous to voltage-sensing domains suggests that the same gating pathway is used by voltage-dependent proton transporters.

The voltage-sensing domains (VSDs) of K+ channels have been shown to undergo large rearrangements during gating, whereas the S4 segment remains positioned between the central pore and the remainder of the VSD in both states (Grabe et al., 2007). In the Shaker K+ channel (1.A.1.2.6), mutation of the first arginine residue of the S4 helix to a smaller uncharged residue makes the VSD permeable to ions in the resting conformation ('S4 down'). There are four omega pores per channel, consistent with one conduction path per VSD. Permeating ions from the extracellular medium enter the VSD at its peripheral junction with the pore domain, and then plunge into the core of the VSD in a curved conduction pathway (Tombola et al. 2007).

Amongst the nine voltage-gated K(+) channel (Kv) subunits expressed in Arabidopsis, AtKC1 does not seem to form functional Kv channels. Co-expression of AtKC1 (1.A.1.4.9), AKT1 (1.A.1.4.1) and/or KAT1 (1.A.1.4.7) genes in tobacco mesophyll protoplasts showed that AtKC1 remains in the endoplasmic reticulum unless it is co-expressed with AKT1 (Duby et al., 2008). Heteromeric AtKC1-AKT1 channels display functional properties different from those of homomeric AKT1 channels. In particular, the activation threshold voltage of the former channels is more negative than that of the latter ones preferred to AKT1-AKT1 homodimers during the process of tetramer assembly. Thus, AtKC1 is a Kv subunit, which downregulates the physiological activity of other Kv channel subunits (Duby et al., 2008).

Shaker-type K+ channels in plants display distinct voltage-sensing properties despite sharing sequence and structural similarity. For example, an Arabidopsis K+ channel (SKOR) and a tomato K+ channel (LKT1) share high amino acid sequence similarity and identical domain structures; however, SKOR conducts outward K+ current and is activated by positive membrane potentials (depolarization), whereas LKT1 conducts inward current and is activated by negative membrane potentials (hyperpolarization). The structural basis for the 'opposite' voltage-sensing properties of SKOR and LKT1 was determined in SKOR channel single amino acid mutations that converted the outward-conducting channel into an inward-conducting channel. Domain-swapping and random mutagenesis produced similar results, suggesting functional interactions between several regions of the SKOR protein that lead to specific voltage-sensing properties. Thus, dramatic changes in rectifying properties can be caused by single amino acid mutations.

The structure of the transmembrane regions of the bacterial cyclic nucleotide-regulated channel MlotiK1 (TC# 1.A.1.25.1), a non-voltage-gated 6 TM channel, has been determined (Clayton et al., 2008). The S1-S4 domain and its associated linker serve as a clamp to constrain the gate of the pore and possibly function in concert with ligand-binding domains to regulate the opening of the pore. Motions of the S6 inner helices can gate the ion conduction pathway at a position along the pore closer to the selectivity filter than the canonical helix bundle crossing.

Carbon monoxide (CO) is a lethal gas, but it is also a physiological signaling molecule capable of regulating a variety of proteins. Among them, large-conductance Ca2+- and voltage-gated K+ (Slo1 BK) channels, important in vasodilation and neuronal firing, have been suggested to be directly stimulated by CO. In fact, CO activates Slo1 BK channels (Hou et al, 2008) in the absence of Ca2+ in a voltage-sensor-independent manner. The stimulatory action of CO requires an aspartic acid and two histidine residues located in the cytoplasmic RCK1 domain. CO probably acts as a partial agonist for the high-affinity divalent cation sensor in the RCK1 domain of the Slo1 BK channel (1.A.1.3.2).

Ca2+-activated BK channels (e.g., 1.A.1.3.3) modulate neuronal activities, including spike frequency adaptation and synaptic transmission. Ca2+-binding sites and the activation gate are spatially separated in the channel protein. By studying an Asp-to-Gly mutation (D434G) associated with human syndrome of generalized epilepsy and paroxysmal dyskinesia (GEPD), Yang et al. (2010) showed that a cytosolic motif immediately following the activation gate S6 helix, known as the AC region, mediates the allosteric coupling between Ca2+ binding and channel opening. The GEPD mutation inside the AC region increases BK channel activity by enhancing this allosteric coupling. Ca2+ sensitivity is enhanced by increases in solution viscosity that reduce protein dynamics. The GEPD mutation alters such a response, suggesting that a less flexible AC region may be more effective in coupling Ca2+ binding to channel opening.

The voltage sensors in VIC family cation channels use a sliding-helix mechanism for electromechanical coupling in which outward movement of gating charges in the S4 transmembrane segments catalyzed by sequential formation of ion pairs pulls the S4-S5 linker, bends the S6 segment, and opens the pore (Catterall, 2010). Impairment of voltage-sensor function by mutations in Na+ channels contributes to several ion channelopathies, and gating pore current conducted by mutant voltage sensors in Na(V)1.4 channels is the primary pathophysiological mechanism in hypokalemic periodic paralysis.

In animals, calcium regulates heartbeat, muscle contraction, neuronal communication, hormone release, cell division, and gene transcription. Major entryways for Ca2+ in excitable cells are high-voltage activated (HVA) Ca2+ channels, Cav (Buraei and Yang, 2010). These are plasma membrane proteins composed of several subunits, including α1, α2δ, β, and γ. Although the principal α1 subunit contains the channel pore, gating machinery and most drug binding sites, the cytosolic auxiliary β subunit plays an essential role in regulating the surface expression and gating properties of HVA Ca2+ channels. Cavβ is also crucial for the modulation of HVA Ca2+ channels by G proteins, kinases, and the Ras-related RGK GTPases. Additional proteins modulate HVA Ca2+ channels by binding to Cavβ, and it may carry out Ca2+ channel-independent functions, including directly regulating gene transcription. All four subtypes of Cavβ, encoded by different genes, have a modular organization, consisting of three variable regions, a conserved guanylate kinase (GK) domain, and a conserved Src-homology 3 (SH3) domain, placing them into the membrane-associated guanylate kinase (MAGUK) protein family. Crystal structures of Cavβs reveal how they interact with Cavα1 (Buraei and Yang, 2010).

Regulator of K+ conductance (RCK) domains control the activity of a variety of K+ transporters and channels, including the human large conductance Ca2+-activated K+ channel that is important for blood pressure regulation and control of neuronal firing, and MthK, a prokaryotic Ca2+-gated K+ channel that has yielded structural insight toward mechanisms of RCK domain-controlled channel gating. In MthK, a gating ring of eight RCK domains regulates channel activation by Ca2+. Pau et al. (2011) showed that each RCK domain contributes to three different regulatory Ca2+-binding sites, two of which are located at the interfaces between adjacent RCK domains. The additional Ca2+-binding sites, resulting in a stoichiometry of 24 Ca2+ions per channel, is consistent with the steep relation between [Ca2+] and MthK channel activity. Comparison of Ca2+-bound and unliganded RCK domains suggests a physical mechanism for Ca2+-dependent conformational changes that underlie gating in this class of channels.

The mechanism of ion channel voltage gating - how channels open and close in response to voltage changes - has been debated since Hodgkin and Huxley's seminal discovery that the crux of nerve conduction is ion flow across cellular membranes. Using all-atom molecular dynamics simulations, Jensen et al. (2012) showed how a voltage-gated potassium channel (KV) switches between activated and deactivated states. On deactivation, pore hydrophobic collapse rapidly halts ion flow. Subsequent voltage-sensing domain (VSD) relaxation, including inward, 15-angstrom S4-helix motion, completes the transition. On activation, outward S4 motion tightens the VSD-pore linker, perturbing linker-S6-helix packing. Fluctuations allow water, then potassium ions, to reenter the pore; linker-S6 repacking stabilizes the open pore. Jensen et al. (2012) proposed a mechanistic model for the sodium/potassium/calcium voltage-gated ion channel superfamily that reconciles apparently conflicting experimental data.

In yeast and filamentous fungi, the Ca2+ channel, Cch1 forms a complex with an auxiliary subunit Mid1 to form the active complex (1.A.1.11.10). Mid1 was originally reported to have Ca2+ channel activity because when produced in Chinese hamster ovary cells, it produced channel activity (Kanzaki et al., 1999). However, it is now clear from many studies that Mid1 is required for Cch1-mediated Ca2+ flux and probably has no inherent channel activity (Ma et al., 2011; Martin et al., 2011; Cavinder and Trail, 2012). Mid1 was originally assigned to TC family: 1.A.16, The Yeast Stretch-Activated Cation-selective Ca2+ Channel, Mid1 (Mid1) Family, but this assignment has been deleted from TCDB, and Mid1 proteins have been incorporated into TC subfamily 1.A.1.11.

The generalized transport reaction catalyzed by members of the VIC family is:

cation (out) ⇌ cation (in).

 

This family belongs to the: VIC Superfamily.

References associated with 1.A.1 family:

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